Probing S4 and S5 segment proximity in mammalian hyperpolarization- activated HCN channels by disulfide bridging and Cd2+ coordination

Pflugers Archiv European Journal of Physiology

Volumn 458, Issue 2, 2009, Pages 259-272

  Bell, Damian C ^a,b   Turbendian, Harma K ^a   Valley, Matthew T ^a   Zhou, Lei ^a   Riley, John H ^a   Siegelbaum, Steven A ^a   Tibbs, Gareth R ^a  

^a Columbia University ^*  (United States)

^b ASTRAZENECA   (United Kingdom)

Author keywords

Cross bridge; Cysteine; HCN clones; Pacemaker; Voltage gating

Indexed keywords

CADMIUM; CYCLIC NUCLEOTIDE GATED CHANNEL; CYSTEINE; DIMER; DISULFIDE; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; POTASSIUM CHANNEL KV1.2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOENGINEERING; CHANNEL GATING; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIMERIZATION; DISULFIDE BOND; ELECTRIC POTENTIAL; ELECTRONIC SENSOR; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR PROBE; NONHUMAN; ORIENTATION; OXIDATION; POLARIZATION AND DEPOLARIZATION; PRIORITY JOURNAL; VOLTAGE CLAMP; WESTERN BLOTTING; X RAY;

ANIMALS; CADMIUM; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; CYSTEINE; DISULFIDES; OOCYTES; PATCH-CLAMP TECHNIQUES; PHENANTHROLINES; XENOPUS LAEVIS;

EID: 67349179481     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-008-0613-3     Document Type: Article

References (53)

1. CA Ahern R Horn 2004 Specificity of charge-carrying residues in the voltage sensor of potassium channels J Gen Physiol 123 205 216 (Pubitemid 38282971)
2. CA Ahern R Horn 2005 Focused electric field across the voltage sensor of potassium channels Neuron 48 25 29 (Pubitemid 41384163)
3. KW Au CW Siu CP Lau HF Tse RA Li 2008 Structural and functional determinants in the S5-P region of HCN-encoded pacemaker channels revealed by cysteine-scanning substitutions Am J Physiol Cell Physiol 294 C136 144
4. OS Baker HP Larsson LM Mannuzzu EY Isacoff 1998 Three transmembrane conformations and sequence-dependent displacement of the S4 domain in shaker K+ channel gating Neuron 20 1283 1294 (Pubitemid 28293143)
5. DC Bell H Yao RC Saenger JH Riley SA Siegelbaum 2004 Changes in local S4 environment provide a voltage-sensing mechanism for mammalian hyperpolarization-activated HCN channels J Gen Physiol 123 5 19 (Pubitemid 38082783)
6. F Bezanilla 2000 The voltage sensor in voltage-dependent ion channels Physiol Rev 80 555 592 (Pubitemid 30164943)
7. F Bezanilla 2005 The voltage-sensor structure in a voltage-gated channel Trends Biochem Sci 30 166 168 (Pubitemid 40463303)
8. A Broomand R Mannikko HP Larsson F Elinder 2003 Molecular movement of the voltage sensor in a K channel J Gen Physiol 122 741 748 (Pubitemid 37517904)
9. FV Campos B Chanda B Roux F Bezanilla 2007 Two atomic constraints unambiguously position the S4 segment relative to S1 and S2 segments in the closed state of Shaker K channel Proc Natl Acad Sci U S A 104 7904 7909 (Pubitemid 47185849)
10. CL Careaga JJ Falke 1992 Thermal motions of surface alpha-helices in the D-galactose chemosensory receptor. Detection by disulfide trapping J Mol Biol 226 1219 1235
11. JM Castagnetto SW Hennessy VA Roberts ED Getzoff JA Tainer ME Pique 2002 MDB: the Metalloprotein Database and Browser at The Scripps Research Institute Nucleic Acids Res 30 379 382 (Pubitemid 34679590)
12. WA Catterall 1986 Molecular properties of voltage-sensitive sodium channels Annu Rev Biochem 55 953 985 (Pubitemid 16070792)
13. A Cha GE Snyder PR Selvin F Bezanilla 1999 Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy Nature 402 809 813 (Pubitemid 30012527)
14. B Chanda OK Asamoah R Blunck B Roux F Bezanilla 2005 Gating charge displacement in voltage-gated ion channels involves limited transmembrane movement Nature 436 852 856 (Pubitemid 41160644)
15. J Chen JS Mitcheson M Tristani-Firouzi M Lin MC Sanguinetti 2001 The S4-S5 linker couples voltage sensing and activation of pacemaker channels Proc Natl Acad Sci U S A 98 11277 11282 (Pubitemid 32928719)
16. N Decher J Chen MC Sanguinetti 2004 Voltage-dependent gating of hyperpolarization-activated, cyclic nucleotide-gated pacemaker channels: molecular coupling between the S4-S5 and C-linkers J Biol Chem 279 13859 13865 (Pubitemid 38468918)
17. F Elinder J Nilsson P Arhem 2007 On the opening of voltage-gated ion channels Physiol Behav 92 1 7 (Pubitemid 47374245)
18. DJ Elliott EJ Neale Q Aziz JP Dunham TS Munsey M Hunter A Sivaprasadarao 2004 Molecular mechanism of voltage sensor movements in a potassium channel EMBO J 23 4717 4726 (Pubitemid 40069702)
19. A Giorgetti P Carloni P Mistrik V Torre 2005 A homology model of the pore region of HCN channels Biophys J 89 932 944 (Pubitemid 41098979)
20. KS Glauner LM Mannuzzu CS Gandhi EY Isacoff 1999 Spectroscopic mapping of voltage sensor movement in the Shaker potassium channel Nature 402 813 817 (Pubitemid 30012528)
21. M Grabe HC Lai M Jain YN Jan LY Jan 2007 Structure prediction for the down state of a potassium channel voltage sensor Nature 445 550 553 (Pubitemid 46197636)
22. HR Guy P Seetharamulu 1986 Molecular model of the action potential sodium channel Proc Natl Acad Sci U S A 83 508 512 (Pubitemid 16080043)
23. Y Jiang V Ruta J Chen A Lee R MacKinnon 2003 The principle of gating charge movement in a voltage-dependent K+ channel Nature 423 42 48 (Pubitemid 36569578)
24. HC Lai M Grabe YN Jan LY Jan 2005 The S4 voltage sensor packs against the pore domain in the KAT1 voltage-gated potassium channel Neuron 47 395 406 (Pubitemid 41073880)
25. M Laine MC Lin JP Bannister WR Silverman AF Mock B Roux DM Papazian 2003 Atomic proximity between S4 segment and pore domain in Shaker potassium channels Neuron 39 467 481 (Pubitemid 36937048)
26. HP Larsson OS Baker DS Dhillon EY Isacoff 1996 Transmembrane movement of the shaker K+ channel S4 Neuron 16 387 397 (Pubitemid 26072371)
27. A Lewis V Jogini L Blachowicz M Laine B Roux 2008 Atomic constraints between the voltage sensor and the pore domain in a voltage-gated K+ channel of known structure J Gen Physiol 131 549 561
28. ER Liman P Hess F Weaver G Koren 1991 Voltage-sensing residues in the S4 region of a mammalian K+ channel Nature 353 752 756 (Pubitemid 21912613)
29. ER Liman J Tytgat P Hess 1992 Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs Neuron 9 861 871
30. DE Logothetis S Movahedi C Satler K Lindpaintner B Nadal-Ginard 1992 Incremental reductions of positive charge within the S4 region of a voltage-gated K+ channel result in corresponding decreases in gating charge Neuron 8 531 540
31. SB Long EB Campbell R Mackinnon 2005 Crystal structure of a mammalian voltage-dependent Shaker family K+ channel Science 309 897 903 (Pubitemid 41099919)
32. SB Long EB Campbell R Mackinnon 2005 Voltage sensor of Kv1.2: structural basis of electromechanical coupling Science 309 903 908 (Pubitemid 41099920)
33. SB Long X Tao EB Campbell R MacKinnon 2007 Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment Nature 450 376 382 (Pubitemid 350126743)
34. A Ludwig X Zong M Jeglitsch F Hofmann M Biel 1998 A family of hyperpolarization-activated mammalian cation channels Nature 393 587 591 (Pubitemid 28319249)
35. R Männikkö F Elinder HP Larsson 2002 Voltage-sensing mechanism is conserved among ion channels gated by opposite voltages Nature 419 837 841 (Pubitemid 35238569)
36. EJ Neale DJ Elliott M Hunter A Sivaprasadarao 2003 Evidence for intersubunit interactions between S4 and S5 transmembrane segments of the Shaker potassium channel J Biol Chem 278 29079 29085 (Pubitemid 36935822)
37. DM Papazian LC Timpe YN Jan LY Jan 1991 Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence Nature 349 305 310 (Pubitemid 21912066)
38. MM Pathak V Yarov-Yarovoy G Agarwal B Roux P Barth S Kohout F Tombola EY Isacoff 2007 Closing in on the resting state of the Shaker K(+) channel Neuron 56 124 140 (Pubitemid 47484186)
39. DJ Posson P Ge C Miller F Bezanilla PR Selvin 2005 Small vertical movement of a K+ channel voltage sensor measured with luminescence energy transfer Nature 436 848 851 (Pubitemid 41160643)
40. DL Prole G Yellen 2006 Reversal of HCN channel voltage dependence via bridging of the S4-S5 linker and post-S6 J Gen Physiol 128 273 282 (Pubitemid 44306707)
41. RB Robinson SA Siegelbaum 2003 Hyperpolarization-activated cation currents: from molecules to physiological function Annu Rev Physiol 65 453 480 (Pubitemid 38249163)
42. L Rulisek J Vondrasek 1998 Coordination geometries of selected transition metal ions (Co2+, Ni2+, Cu2+, Zn2+, Cd2+, and Hg2+) in metalloproteins J Inorg Biochem 71 115 127
43. V Ruta J Chen R MacKinnon 2005 Calibrated measurement of gating-charge arginine displacement in the KvAP voltage-dependent K+ channel Cell 123 463 475 (Pubitemid 41546676)
44. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
45. B Santoro DT Liu H Yao D Bartsch ER Kandel SA Siegelbaum GR Tibbs 1998 Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain Cell 93 717 729 (Pubitemid 28257579)
46. B Santoro GR Tibbs 1999 The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels Ann N Y Acad Sci 868 741 764 (Pubitemid 29281192)
47. F Sesti S Rajan R Gonzalez-Colaso N Nikolaeva SA Goldstein 2003 Hyperpolarization moves S4 sensors inward to open MVP, a methanococcal voltage-gated potassium channel Nat Neurosci 6 353 361 (Pubitemid 36373980)
48. DM Starace F Bezanilla 2004 A proton pore in a potassium channel voltage sensor reveals a focused electric field Nature 427 548 553 (Pubitemid 38209113)
49. F Tombola MM Pathak EY Isacoff 2006 How does voltage open an ion channel? Annu Rev Cell Dev Biol 22 23 52
50. S Vemana S Pandey HP Larsson 2004 S4 movement in a mammalian HCN channel J Gen Physiol 123 21 32 (Pubitemid 38082784)
51. N Yang AL George Jr R Horn 1996 Molecular basis of charge movement in voltage-gated sodium channels Neuron 16 113 122 (Pubitemid 26044734)
52. V Yarov-Yarovoy D Baker WA Catterall 2006 Voltage sensor conformations in the open and closed states in ROSETTA structural models of K(+) channels Proc Natl Acad Sci U S A 103 7292 7297 (Pubitemid 43727826)
53. SP Yusaf D Wray A Sivaprasadarao 1996 Measurement of the movement of the S4 segment during the activation of a voltage-gated potassium channel Pflugers Arch 433 91 97 (Pubitemid 26405626)